Chronic diseases and multimorbidity are common in western countries and associated with increased breast cancer mortality. This study aims to investigate non-participation in breast cancer screening among women with chronic diseases and multimorbidity and the role of time in this association.
Trang 1R E S E A R C H A R T I C L E Open Access
Non-participation in breast cancer screening
for women with chronic diseases and
multimorbidity: a population-based cohort study
L F Jensen1,2,3,4*, A F Pedersen1,3, B Andersen4, M Vestergaard1,2and P Vedsted1,3
Abstract
Background: Chronic diseases and multimorbidity are common in western countries and associated with increased breast cancer mortality This study aims to investigate non-participation in breast cancer screening among women with chronic diseases and multimorbidity and the role of time in this association
Method: This population-based cohort study used regional and national registries Women who were invited to the first breast cancer screening round in the Central Denmark Region in 2008–09 were included (n = 149,234) Selected chronic diseases and multimorbidity were assessed up to 10 years before the screening date Prevalence ratios (PR) were used as an association measure
Results: The results indicated that women with at least one chronic condition were significantly more likely not to participate in breast cancer screening In adjusted analysis, a significantly higher likelihood of non-participation was found for women with cancer (PR = 1.50, 95 % CI: 1.40–1.60), mental illness (PR = 1.51, 95 % CI: 1.42–1.60), chronic obstructive pulmonary disease (PR = 1.51, 95 % CI: 1.42–1.62), neurological disorders (PR = 1.24, 95 % CI: 1.12–1.37) and kidney disease (PR = 1.70, 95 % CI 1.49–1.94), whereas women with chronic bowel disease (PR = 0.75, 95 % CI 0.65–0.88) were more likely to participate than women without these disease Multimorbidity was associated with increased non-participation likelihood E.g having 3 or more diseases was associated with 58 % increased non-participation likelihood (95 % CI: 27–96 %) Higher non-participation was also observed for women with severe multimorbidity (PR = 1.53, 95 % CI: 1.23–1.90) and mental-physical multimorbidity (PR = 1.54, 95 % CI: 1.36–1.75)
Conclusion: In conclusion, we found a strong association between non-participation in breast cancer screening for some chronic diseases and for multimorbidity The highest propensity not to participate was observed for women with hospital contacts related to the chronic disease in the period closest to the screening date
Keywords: Chronic disease, Multimorbidity, Breast cancer screening, Mammography screening, Participation, Non-attendance, Denmark
Background
Breast cancer is the second most common cancer type
worldwide and the most common cancer type among
Danish women [1, 2] Breast cancer screening can detect
breast cancer at an early stage where the prognosis for
survival is better [3] Breast cancer screening has
there-fore been introduced as a universal programme in many
western countries In Denmark, women between 50 and
69 years of age are invited biennially to a mammogram free of charge [3]
A growing proportion of people are living with chronic diseases and multimorbidity [4, 5] Studies have found that comorbidity increases the mortality risk among breast cancer patients [6, 7] which in some studies have been related to the comorbidities rather than to the breast cancer [6, 8] Yet, the cancer prognosis depends on the disease stage at the time of diagnosis [3], and given the in-creased mortality rate among breast cancer patients with
* Correspondence: line.jensen@ph.au.dk
1
Department of Public Health, The Research Unit for General Practice, Aarhus
University, Bartholins Allé 2, 8000 Aarhus C, Denmark
2
Department of Public Health, Section for General Practice, Aarhus University,
Bartholins Allé 2, 8000 Aarhus C, Denmark
Full list of author information is available at the end of the article
© 2015 Jensen et al Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made The Creative Commons Public Domain Dedication waiver
Trang 2chronic diseases, this group may benefit particularly from
early diagnosis
The association between chronic diseases,
multimor-bidity and non-participation in breast cancer screening
has not been studied sufficiently [9, 10] Some studies
have investigated diseases individually and their results
are not consistent [9–14] Five studies found that
multi-morbidity increased non-participation [9, 13, 15–17],
but Heflin et al [10] found in their study that three or
more conditions increased the propensity to participate
Although chronic diseases are long-lasting by
defin-ition, patients may experience periods where the disease
is not followed at hospital but rather by primary care,
e.g., during a stable disease period [18] We hypothesised
that being diagnosed with diseases that involve hospital
contact close to the screening date affects screening
behaviour more than the presence of chronic diseases
without recent hospital contact To our knowledge, this
issue has not been studied before
This study has two purposes: first, to analyse whether
being diagnosed with specific chronic diseases or with
multimorbidity is associated with non-participation in
breast cancer screening and, second, to study whether
any such association varies with respect to the time that
has elapsed since the disease required contact to the
hospital sector with the investigated diseases We
hypothesised that women with chronic diseases and
multimorbidity were more likely not to participation
Methods
Setting
The setting for the study was the Central Denmark
Region (1.2 million inhabitants, approx 150,000 women
aged 50–69) Breast cancer screening was introduced as
an organised, universal and free-of-charge programme in
2008–09 in the Central Denmark Region where 78.9 %
of the invited women participated [19]
Study design and population
We conducted an observational, registry-based,
histor-ical cohort study with screening participation as the
outcome and we assessed registrations of chronic
dis-eases up to ten years before the scheduled screening
date The population comprised women invited to the
first organised breast cancer screening round in the
Central Denmark Region in 2008–09 (N = 149,234)
and we excluded women who were dead or have
moved between the invitations were send out and the
screening date or were outside the caption area (n = 324)
and women with registration of breast cancer in the Danish
Cancer Registry [20] (n = 4,646) In total, 144,264 women
were included; see more information in our previous
publication [19]
Data collection and variables
Information on participation in breast cancer screening was obtained from a regional administrative database containing individual information on, e.g., participation status, the scheduled screening date and the unique cen-tral registration number (CRN) possessed by all Danes [21] The present study is based on data from the preva-lent screening round in the Central Denmark Region Hence, a woman was defined as a participant if she had participated in the first organised breast cancer screening round in the Central Denmark Region and as a non-participant if she had not
All data described in this section were linked using the unique CRN number [21]
Data on chronic diseases were drawn from the Danish National Patient Registry (NPR) [22] The registry was founded in 1977 and initially included admission infor-mation Since 1995, the registry has expanded to include information on all outpatient and emergency contacts All contacts are registered with a main diagnosis (i.e ac-tion diagnosis) based on the Internaac-tional Classificaac-tion
of Diseases, 10th version (ICD-10) [22] Data on psychi-atric diseases were drawn from the Danish Psychipsychi-atric Central Research Register (PCRR) All Danish psychiatric departments document every contact to the PCRR, and ICD-10 codes for each hospital admission, outpatient and emergency contacts were available for the entire study period [23]
The chronic diseases of interest were selected based
on a recent literature review [24], which recommended the inclusion of 11 core chronic diseases when assessing multimorbidity Based on their recommendations and another study in the field [25], we included a larger number of specific chronic diseases and grouped these diseases into 11 comprehensive chronic disease groups (CDGs) on which data were drawn from the NPR and the PCRR The following CDGs were included: diabetes, hypertension, cancer, chronic obstructive pulmonary dis-ease (COPD), cardiovascular disdis-eases, chronic arthritis, chronic kidney disease, chronic liver disease, chronic neurological disorders, chronic bowel disease and chronic mental illness (Additional file 1)
Multimorbidity was operationalised as follows: “Multi-morbidity” covers the co-occurrence of two or more chronic diseases from two or more of the CDGs.“Severe multimorbidity” designates the co-occurrence of three or more chronic diseases from three or more of the CDGs
“Physical multimorbidity” describes the co-occurrence of two or more physical CDGs, but without the mental CDG “Physical-mental multimorbidity” signifies the co-occurrence of at least one physical CDG and the mental CDG Thus, a woman could be categorised as having more than one type of multimorbidity; e.g severe multimorbidity and physical multimorbidity Finally, we measured“disease
Trang 3counts” within the categories: 0, 1, 2, ≥3 CDGs, with the
latter category being combined due to few occurrences
Study participants were categorised with one of the
diseases mentioned above if they had an emergency
con-tact, an outpatient contact or an admission with one of
the selected diseases to any Danish hospital during the
10 years period before screening We intended to study
if an association varied with time as we hypothesised
that the likelihood of non-participation would be
stron-ger for women with a chronic disease requiring hospital
attention in the period leading up to screening
com-pared to women with chronic diseases that did not
re-quire hospital attention in the period leading up to
screening Because of this, data on the 10-year follow-up
were stratified into two time periods which were not
mutually exclusive: (1) any hospital contact with the
in-cluded chronic diseases≤2 years (i.e 0–730 days) before
the screening date; and (2) hospital contacts with the
in-cluded chronic diseases >2–10 years (i.e 731–3652 days)
before the screening date Thus, a woman could be
cate-gorised in both groups if she was registered in the NPR
or PCRR with a given disease in both time periods
E.g.55 % of all women was registered with rheumatoid
arthritis in both time periods (data not shown)
We obtained individual data on the population’s
socio-economic position (SEP) registered the year of the
scheduled screening date from Statistics Denmark [26]
and included: ethnicity categorised as 1) Danish and
de-scendants of immigrants and 2) immigrants Marital
status was categorised as married/cohabitating and
sin-gle Education was classified according to the UNESCO
classification [27] as low (≤10 years), middle (11–15
years) and higher (>15 years) Finally, age on the date of
the scheduled screening was included as a continuous
variable in the multivariate analyses
Finally, almost all Danish citizens (98 %) are listed with
a specific general practitioner (GP) or general practice
[28], and data on GP attachment were obtained from the
Danish National Health Service Registry which was used
to do cluster adjustments by GP affiliation
Statistical analysis
All analyses were performed using Stata 13.1 Prevalence
ratios (PRs) with 95 % confidence intervals (95 % CI)
were estimated using generalised linear models (GLM)
[29, 30] PRs were chosen over the odds ratio, as it has
been found to overestimate associations when the
out-come is frequent [30]
Unadjusted analyses were conducted for each of the
CDGs We compared women having each specific CDG
with women without the CDG in question In model 1,
we adjusted for SEP (ethnicity, marital status, education
and age) In model 2, we adjusted for the variables in
model 1 (SEP) and for the coexistence of the other
included diseases We also hypothesised that an associ-ation between one given disease and non-participassoci-ation
in one time period could be confounded by having chronic diseases in the other time period Therefore, we also adjusted model 2 for being registered in the NPR or PCRR in the other time period
Unadjusted analyses were also conducted for the mul-timorbidity variables Model 1 adjusted for SEP (ethni-city, marital status, education and age) Model 2 adjusted for the variables in model 1 (SEP) and for being registered in the NPR or PCRR with multimorbidity in the other time period E.g when studying severe multi-morbidity >2–10 years before the scheduled screening date, we adjusted for SEP and for having severe multi-morbidity in the period ≤2 years before the scheduled screening date
We assessed the association between the latest hospital contact with either of the included diseases and non-participation with a cubic spline model, using the method proposed by Orsini and Greenland and knots were set at 5, 27.5, 50, 72.5 and 95 percentiles [31, 32] All analyses were assessed with robust variance esti-mates to adjust for clustering of patients in general prac-tices This was done as practice clustering might be related to the propensity to be diagnosed with a chronic disease and also to participate in breast can-cer screening [33]
Ethical approvals
No ethical approval was required according to Danish legislation and the National Committee on Health Research Ethics in the Central Denmark Region as the study was based on registry and survey data (j no 181/ 2011) Approval for data on screening behaviour was granted from the Central Denmark Regions legal depart-ment (j no.: 1-16-02-109-09) and permission for the na-tional registry data was granted from by the Danish Data Protection Agency (j no.: 2009-41-3471)
Results Study population social-characteristics
A higher non-participation proportion was found among women in the oldest age group, single women, women with non-Danish origin and with low educa-tion (Table 1)
CDGs and non-participation in breast cancer screening
In total, 20.3 % of women without a chronic disease did not participate in the first screening round whereas 28.6 % women with minimum one of the chronic dis-eases did not participate (Table 1) For most of the CDGs, women who had a chronic condition were more inclined to abstain from participation than women who had no chronic diseases except for hypertension and
Trang 4chronic arthritis The participation proportion was
higher for women with chronic bowel disease than for
women without chronic bowel disease (Table 2)
In model 2, having cancer, mental illness, COPD, chronic
neurological disorder and chronic kidney disease
signifi-cantly increased the likelihood of non-participation in both
time periods, whereas having bowel disease increased the
likelihood of participation (PRmodel2= 0.75, 95 % CI: 0.65–
0.88) (Table 3) Diabetes was insignificantly related to
screening≤2 years before the screening date; but if the
lat-est hospital contact was between >2–10 years before the
screening date, women with diabetes were significantly less
likely to participate For women with chronic liver disease
and cardiovascular disease, non-participation became
insig-nificant in model 2 Hypertension and chronic arthritis
were significantly associated with higher participation if
the last hospital contact was >2–10 years before the
screening date, but not if it was≤2 years before screening
(Table 3)
Multimorbidity and non-participation in breast cancer
screening
Overall, non-participation was more common among
women with multimorbidity and a higher disease count
(Table 4) In the regression analyses, the disease-count variable showed an increased non-participation likelihood with each additional disease compared with no disease (e.g 3 diseases: PRmodel 2= 1.58, 95 % CI: 1.27–1.96) (Table 5) Women with any of the multimorbidity aspects were significantly more likely not to participate than were women without multimorbidity This applied in both time periods, but the estimates were highest for hospital con-tact≤2 years before the screening date In general, the as-sociations between the different types of multimorbidity and non-participation were largely similar However, hav-ing severe multimorbidity (≥3 diseases) was associated with a somewhat higher non-participation propensity (PRmodel2= 1.53, 95 % CI: 1.23–1.90) than having multi-morbidity (≥2 diseases) (PRmodel2= 1.38, 95 % CI: 1.29– 1.49) Non-participation likelihood was also somewhat higher for women with physical-mental multimorbidity than women with physical multimorbidity (PRmodel2= 1.54, 95 % CI: 1.36–1.75 and PRmodel2= 1.37, 95 % CI: 1.26–1.49, respectively) (Table 5)
The association between the latest hospital contacts with any of the included diseases indicated a non-linear association Non-participation was highest when the latest hospital occurred in the year leading up to screening and the PR of non-participation did not dif-fer markedly if the latest hospital contact occurred 6
or more years before screening (data not shown)
Discussion
This large population-based cohort study revealed that women with cancer, mental illness, COPD, neurological disorders or kidney disease had an increased likelihood
of non-participation in breast cancer screening The like-lihood of non-participation increased with the number
of co-existing diseases and was particularly high for women with severe multimorbidity and mental-physical multimorbidity The associations were in general stron-gest when the women had hospital based contacts with the disease in the period≤2 years before screening com-pared to when the contacts had occurred > 2 to 10 years before screening Sub-analysis indicated that the likeli-hood of non-participation was affected the most if the latest hospital contact occurred up to one year before screening
Strengths and limitations
Data on screening participation were obtained from an administrative registry with no missing information and
no reliance on self-reported data The cohort comprised
a well-defined population, i.e the prevalent screening round in the Central Denmark Region; and using the CRN, we were able to identify and follow the entire population and can therefore exclude selection bias
Table 1 Socio-economic position of the study population
divided according to participation in the screening programme
(n = 144,264, numbers vary due to missing observations)
All women
Participants Non-participants P-value
(chi 2 )
113,811 (79.1) 30,453 (21.1)
Married/cohabiting 88,590 (82.7) 18,484 (17.3)
Danish/descendant 110,018 (79.6) 28,201 (18.3)
(n = 144,264, numbers vary due to missing observations)
a
Presence of chronic diseases ≤2 years before the scheduled screening date
Trang 5We included chronic diseases as registered in nationwide
registries containing information on all hospital-related
contacts in Denmark [22, 23] The validity of the registries
has been established for several of the included diseases
[34–36] However, these registers do not contain
informa-tion on treatment in general practice; thus the results of
this study apply only to patients with hospital-requiring
treatment Patients who are treated only in general practice will in our analysis appear in the reference group but be-cause our reference group is very large this proportion will presumably be small and will probably not affect the results markedly As no Danish registers contains data on routine treatment from general practice, it was not possible to study or adjust for this in the present study
Table 2 Distribution of women with the selected CDGs≤2 years and >2–10 years before screening and screening participation (n = 144,264)
Contacts to hospital with the CDGs ≤2 years before the screening date
Contacts to hospital with the CDGs >2 –10 years before the screening date
Trang 6In this study, chronic diseases and multimorbidity
were specified based on leading studies in the field
[24, 25] However, generalisations cannot be made
about chronic diseases in general as the study included
only some and not all existing chronic diseases The
chronic diseases that were selected were categorised into
groups of chronic diseases (see Additional file 1) since we believe that the practical implications of the results would
be relevant to more people Moreover, combining, e.g., several mental diseases with a varying degree of severity and chronicity might lead to less nuanced findings for this group of patients
Table 3 PR of screening non-participation by the selected CDGs≤2 years and >2–10 years before screening (n = 144,264)
Cardiovascular diseases
Cancer
Hypertension
Chronic mental illness
Diabetes
Chronic obstructive pulmonary disease
Chronic neurological disorders
Chronic arthritis
Chronic bowel disease
Chronic liver disease
Chronic kidney disease
a
Adjusted for age, ethnicity, marital status and education
b
Adjusted for age, ethnicity, marital status, education, for being registered in the NPR or PCRR with the other studied chronic diseases, and for being registered in the NPR or PCRR with one of the CDGs in the other time period (yes/no) E.g cancer 0 –2 year before screening is adjusted for SEP, for the remaining 10 studied diseases and for being in hospital contact with one of the 11 included chronic disease groups >2 –10 years before screening
Statistically significant results in bold
Trang 7Chronic diseases, multimorbidity and screening behaviour
A previous cancer diagnosis (other than breast cancer)
was related to non-participation in both time periods
Several explanations for this finding can be suggested
First of all, some women may have attended a
post-cancer follow-up programme and therefore did not find
it relevant to participate in screening Others may have
been too ill to participate, or they may have been in a
palliative phase Some may have been unrealistically
op-timistic [37] and may not have perceived themselves as
being at risk of being diagnosed with yet another type of
cancer Conversely, others may have avoided anything
relating to cancer because of the trauma experienced by
having the first cancer diagnosis Notwithstanding, it has
been shown that some previous cancer types increases
the risk of developing later breast cancer [38–40], which
makes these results important as this group may benefit
particularly from early detection of cancer
Having chronic bowel disease was the only CDG that
significantly increased the propensity to participate in
breast cancer screening in both time periods Chronic
bowel disease often has an early onset in life compared
with the other included diseases and being diagnosed
with this disease often involves continuous health-care
follow-up These women may therefore have been
‘schooled’ from early on in life to engage in healthy
life-styles and may be used to having various contacts with
the healthcare system and undergoing tests [41, 42] A study from 2014 also found higher likelihood of having followed a recommended breast cancer screening programme among women with digestive disease com-pared to women without any digestive disease [13] Taken together, this seems to indicate that having a bowel/digestive-related disease has a positive impact on screening behaviour Having cardiovascular diseases was not associated with non-participation after adjustments,
a finding which is supported by other studies [11, 43] but not all [13] Having hypertension, chronic arthritis and diabetes up to 2 years before screening were not as-sociated with screening participation However, if the lat-est contact was >2–10 years before screening, having hypertension and arthritis increased participation signifi-cantly, and having diabetes increased non-participation The underlying mechanisms here are unclear, but they could, e.g., be related to these women’s lifestyles, an issue which should be studied further
This study shows that having multimorbidity increases non-participation This is supported by five other studies [9, 13, 15–17], even if one of these studies found an as-sociation for women ≥75 years only [17] Another study, conducted in the USA and based on self-reported data, found the opposite; namely that multimorbidity increased participation [10] The authors argue that women with multimorbidity have more frequent contact with the GP
Table 4 Distribution of women with multimorbidity≤2 years and >2–10 years before screening and their participation status (n = 144,264)
Contacts to hospital with the CDGs ≤2 years
before the screening date
Contacts to hospital with the CDGs >2 –10 years before the screening date
Trang 8who plays a direct role in advising women to participate in
screening in the USA [10] However, the other studies
which found the opposite were also conducted in the USA
The association between chronic diseases, multimorbidity
and non-participation may be explained by several factors
Women with one or more chronic diseases may not feel
well enough to participate, and the competing demands in
relation to managing their chronic disease(s) may take up
all their energy [9, 18] It has also been raised as a possible
explanation that non-participation among diseased women
is based on deliberate decisions from the patient (or their
GP) based on an evaluation of costs and benefits, taking
into account the severity of the disease, reduced quality of
life and shortened life expectancy [9, 15]
This study is the first to include different time periods
for hospital contacts For most diseases and all aspects
of multimorbidity, the estimates were strongest for
the≤ 2 year period before the screening date Some studies
have adjusted for e.g.“number of years with illness/in
con-tact with clinic” or “number of concon-tacts” [9, 13, 15, 16],
but no study has evaluated whether the associations
de-pend on elapsing time since last hospital contact Thus,
these results add to the current literature as it highlights
that non-participation is especially challenged when the
woman is affected by the disease in the period leading up
to the screening appointment
This study clearly indicates that women with some of the studied chronic diseases and women with multimor-bidity are not engaging in screening to the same extent
as their female counterparts who do not have the se-lected CDGs and multimorbidity As these women are more frequently in contact with the health care system, this may make it easier to inform them about the advan-tages of screening for early diagnosis This group of women may also derive particular benefits from their general practitioner playing a more active role discussing with them the pros and cons of breast cancer screening
Conclusion
In conclusion, this study indicates increased non-participation in breast cancer screening for women who previously have been in contact with the second-ary healthcare system for some of the selected CDGs Non-participation was strongly associated with having multimorbidity Strongest associations were found when the hospital contacts for the diseases had oc-curred in the recent period before screening Women suffering from chronic diseases or multimorbidity may achieve health gains from early detection of cancer owing to their participation in screening; and their participation could with possible benefit be encouraged
by healthcare professionals
Table 5 PR of screening non-participation by multimorbidity≤2 years and >2–10 years before screening (n = 144,264)
Disease count
Multimorbidity ( ≥2 diseases)
Severe multimorbidity ( ≥3 diseases)
Physical multimorbidity
Physical-mental multimorbidity
a
Adjusted for age, ethnicity, marital status and education
b
Adjusted for age, ethnicity, marital status, education, and for being registered in the NPR or PCRR with the studied multimorbidity in the other time period (yes/ no) E.g severe multimorbidity 0 –2 year is adjusted for SEP, and for being in hospital contact with 3 or more chronic disease groups >2-10 years before screening Statistically significant results in bold
Trang 9Additional file
Additional file 1: Selected chronic disease groups and the
included diseases in each group together with their ICD-10
codes [24, 25, 37, 44 –47] (DOCX 18 kb)
Abbreviations
CDG: Chronic disease group; CI: Confidence interval; COPD: Chronic
Obstructive Pulmonary Disease; CRN: Civil registration number;
GLM: Generalised linear models; GP: General practitioner; ICD-10: The
International Classification of Diseases, 10th version; NPR: National Patient
Registry; PCRR: Danish Psychiatric Central Research Register; PR: Prevalence ratio;
SEP: Socio-economic position.
Competing interests
The authors declare that there are no conflicts of interests.
Authors ’ contribution
AFP, BA, LFJ, and PV conceived the idea LFJ, PV, AFP, MV and BA contributed
with input and critical revision of the statistical analyses and the contents of the
paper LFJ was primarily responsible for drafting the manuscript and for the
statistical analyses All authors read and approved the final version manuscript.
Acknowledgements
We would like to thank the Danish Cancer Society, the Novo Nordic
Foundation, the Riisfort Foundation, the Health Research Fund of Central
Denmark Region and the Faculty of Health, Aarhus University, for the financial
support that made this project possible MV is supported by an unrestricted
grant from the Lundbeck Foundation (grant number: R155-2012-11280).
Author details
1 Department of Public Health, The Research Unit for General Practice, Aarhus
University, Bartholins Allé 2, 8000 Aarhus C, Denmark 2 Department of Public
Health, Section for General Practice, Aarhus University, Bartholins Allé 2, 8000
Aarhus C, Denmark 3 Department of Public Health, The Research Centre for
Cancer Diagnosis in Primary Care (CaP), Aarhus University, Bartholins Allé 2,
8000 Aarhus C, Denmark 4 Department for Public Health Programs, Regional
Hospital of Randers, Skovlyvej 1, 8930 Randers, Denmark.
Received: 11 July 2015 Accepted: 18 October 2015
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